Early Age at Menarche and Allostatic Load: Data from the

Third National Health and Nutrition Examination Survey

JENIFER E. ALLSWORTH, PHD, SHERRY WEITZEN, PHD,
AND LORI A. BOARDMAN, MD, SCM

PURPOSE: To examine whether there is an association between early age at menarche and allostatic
loadda measure of cumulative biologic riskdusing data from the Third National Health and Nutrition
Examination Survey (NHANES III).
METHODS: A total of 2470 (weighted N Z 25,544,838) women aged between 17 and 30 years with
interview and examination data who did not report oral contraceptive use before menarche and were not
missing data on the exposure or outcome were included. Early menarche was defined as menarche at age 10
or younger. The allostatic load score was the sum of the number of 11 components for which an individual
had a value within the high-risk range.
RESULTS: The prevalence of early menarche was 7%. Although the overall allostatic load scores were
low when compared with older adults, the mean allostatic load score was higher among those with
menarche at ages 10 or younger compared with those with later ages at menarche (1.99 vs. 1.33). After
adjusting for age, race/ethnicity, level of education, household poverty income ratio, smoking, and
depression history, women with high allostatic load scores had more than 2 times the odds as those with low
scores of experiencing menarche at age 10 or earlier (OR Z 2.18; 95% CI, 1.293.68).
CONCLUSIONS: This study is the first to report and examine the relationship between age at menarche
and allostatic load. Future studies involving prospective measurement of allostatic load biomarkers may
prove essential for disentangling the association between allostatic load and early age at menarche.
Ann Epidemiol 2005;15:438444. 2005 Elsevier Inc. All rights reserved.
KEY WORDS:

Menarche, Menstrual Cycle, Reproductive Health, Womens Health, Stress, Psychological.

INTRODUCTION
Menarche, the beginning of menstrual function, is a milestone in womens lives. In addition to signaling the start of
the reproductive phase, age at menarche is an important
predictor of adolescent, adult, and postmenopausal health.
For example, among adolescents, early age at menarche is
associated with early initiation of sexual activity (1). Age at
menarche may also be associated with cardiovascular disease
(2), and obesity (3) as well as certain cancers (4, 5). The
onset of menarche has been associated with numerous
factors including immutable characteristics such as race/
ethnicity (69), and genetics, as well as such recognized

From the Center for Gerontology and Health Care Research, Department of Community Health, Brown Medical School, Providence, RI
(J.E.A., S.W.); Division of Research, Department of Obstetrics and
Gynecology, Women and Infants Hospital, Providence, RI (S.W.); and
Division of Ambulatory Care, Department of Obstetrics and Gynecology,
Women and Infants Hospital, Providence, RI (L.A.B.).
Address correspondence to: Jenifer E. Allsworth, Ph.D., Center for
Gerontology and Health Care Research, Department of Community
Health, Brown Medical School, Box G-ST, Providence, RI 02912. Tel.:
(401) 863-2501; Fax: (401) 863-3489. E-mail: Jenifer_Allsworth@brown.
edu
Received July 26, 2004; accepted December 8, 2004.
2005 Elsevier Inc. All rights reserved.
360 Park Avenue South, New York, NY 10010

exogenous sources as nutrition and body composition

(10, 11), exercise (10, 12, 13), and environmental exposures
(14). While stress has been clearly linked to menstrual cycle
characteristics (1518), findings related to the association of
stress and timing of menarche have been mixed (1922).
Over the past century, the average age at menarche has
decreased significantly, although the magnitude of this
decrease remains under debate. Freedman and colleagues
(6), using data from a cohort of almost 70,000 female
radiology technologists, estimated average age at menarche
by birth cohort. In this cohort, the age of menarche
decreased among white women from 13.1 years among those
born before 1920 to 12.5 years among those born in the
1940s or later, a decline which appears to have stabilized. In
contrast, although the average age at menarche among black
or Asian women was similar to that of white women in the
early birth cohorts, it continued to decline. In fact, data from
the Bogalusa Heart Study indicate that the rate of early
menarche was 1.4 times faster for black girls when compared
with white girls (9). Other studies support this finding and
confirm this racial/ethnic disparity in age at menarche. For
example, the National Growth and Health Study found that
the average age at menarche was 12.7 years for whites, and
12.0 years for blacks (7). Similarly, analyzing data from the
1047-2797/05/$see front matter
doi:10.1016/j.annepidem.2004.12.010

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Selected Abbreviations and Acronyms

BMI Z body mass index
CI Z confidence interval
HDL Z high density lipoprotein
NHANES Z National Health and Nutrition Examination Survey
OR Z odds ratio

Third National Health and Nutrition Examination Survey

(NHANES III), Chumlea and colleagues (8) reported that
the median age at menarche was 12.6 for whites, 12.1 for
black, and 12.3 years for Mexican American adolescents.
One mechanism linking stressful experiences with
alterations in reproductive function occurs via dysregulation
of the bodys stress responses, particularly the hypothalamicpituitary-adrenal (HPA) axis (23, 24). Multiple studies have
shown that stress can affect HPA axis function including
glucocorticoid secretion (23, 24). In turn, secretion of
glucocorticoids affect ovarian function (25) via the
hypothalamus. The hypothalamus regulates menstrual
function by secreting gonadotropin-releasing hormone in
pulses, which stimulates the periodic release of both follicle
stimulating and luteinizing hormone from the pituitary
gland.
Allostatic load has been defined as the cumulative wear
and tear that occurs in an individual due to exposure to
stress hormones resulting from chronic or repeated challenge (26). The body functions and survives through
constant alterations in physiologic processes in response to
challenge. This process is referred to as allostasis. By
determining allostatic load, we can attempt to quantify
the cumulative wear and tear due to exposure to physical
and psychosocial stressors (27). In previous studies,
allostatic load has been positively associated with socioeconomic position (2830), challenge (30), psychological
distress (31), and hostility (29) while mediated by positive
social relationships (28, 30, 32).
Studies in adults have found that allostatic load is
predictive of both cognitive and functional decline, as well
as mortality (3335). In fact, a recent study found that
allostatic load may explain as much as one-third of the
socioeconomic disparity in mortality risk (36). Although
few studies have been conducted of the impact of allostatic
load earlier in life, studies in children have suggested that
allostatic load is associated with the number of days a child
reports she/he is ill (37).
In this study we sought to examine the association
between allostatic loadda measure of cumulative biologic
riskdwith age at menarche using data from NHANES III.
The composite allostatic load score quantifies physiologic
dysregulation in multiple systems pertinent to disease risk.
Our definition of allostatic loaddbased on that developed

Allsworth et al.
ALLOSTATIC LOAD AND AGE AT MENARCHE

439

by Crimmins and colleagues (38)dreflects metabolic, cardiovascular, renal, pulmonary, and inflammatory activity.
METHODS
Study Population
The association of allostatic load and early age of menarche
was evaluated using data from NHANES III conducted
between the years of 1988 and 1994 by the National Center
for Health Statistics at the Centers for Disease Control and
Prevention. Methods describing this national survey have
been previously published (39). The survey was designed to
obtain nationally representative information on the health
and nutritional status of the population of the United States
through interviews and direct physical examinations. Selfreported health data as well as physiologic measures were
collected in either the Mobile Examination Center or at the
participants homes. Of those included in these analyses,
the overwhelming majority completed their examination at
the Mobile Examination Center; only 3 were examined at
home.
For these analyses, women between the ages of 17 and 30
with interview and examination data were included. The
sample was limited to young women to minimize the
possibility of misclassification of age of menarche. A total of
371 women were excluded from the analyses due to missing
data on age of menarche (n Z 241), oral contraceptive use
before menarche (n Z 4), or missing 6 or more components
that comprise the allostatic load score (n Z 305). The final
sample included data from 2470 women, which when
weighted, represents the experience of 25,544,838 US
women between the ages of 17 and 30.
Early Menarche
The definition of early menarche was created from
data collected through the examination component of
NHANES. Women were asked up to two questions regarding their age at the time of menarche. First, interviewers
asked women to recall their age of menarche. If they were
unsure, they were asked whether their age of menarche fell
in any of these categories: younger than 10, 10 to 12, 13 to
15, or 16 or older. A woman was defined as having experienced early menarche if she reported on either question that
she experienced menarche at age 10 or younger. Given that
there is a significant difference in the mean age at menarche
by race/ethnicity, the operational definition was selected to
have early age at menarche be rare in all groups. Based on
data from Chumlea and colleagues (8), the 10th percentile
was 10.5 years for black, non-Hispanic women and 10.8
years for Mexican American women. The 3 women that
reported that their menarche occurred between the ages of
10 and 12 were not defined as having undergone early
menarche.

440

Allsworth et al.
ALLOSTATIC LOAD AND AGE AT MENARCHE

Allostatic Load
The operational definition of allostatic load chosen for this
analysis was based on that of Crimmins and colleagues (38)
using data from NHANES III. The measure of cumulative
physiologic dysregulation was composed of 11 components:
diastolic blood pressure, systolic blood pressure, glycosylated
hemoglobin, body mass index (BMI), triglycerides, high
density lipoprotein (HDL) cholesterol, total cholesterol,
albumin, C-reactive protein, peak flow, and urinary
creatinine clearance. For each component a binary high
risk category was created; categories were defined by either
clinical guidelines or empirical values (highest or lowest
quartile) based on all adults in NHANES III. Specifically,
clinical guidelines were used to determine cut-points for
systolic and diastolic blood pressure (40); HDL and total
cholesterol (41); and body mass index (42). There are two
differences between our definition and that used by
Crimmins and colleagues (38). Our high-risk category for
triglycerides was defined by both clinical guideline (41) and
empirical cut-point depending on fasting status. Further, our
definition of high risk for total cholesterol (> 240) was
based on that recommended by the National Cholesterol
Education Program (41). For components with missing data
the high-risk indicator was imputed using a random uniform
distribution. Overall the number of imputed values for any
individual component was small; the percentage imputed
ranged from less than 0.1% for BMI to 3.4% for peak flow.
The allostatic load score was the sum of the number of
components for which an individual had a value within the
high-risk range. Scores in this sample ranged between 0 and
8, with a mean of 1.37. High allostatic load was defined as an
allostatic load score in the top quartile (3 or greater).
Detailed information on cut-points, high-risk categories
and means for the individual components are presented in
Table 2, while crude and adjusted associations with early
menarche are presented in Table 3.
Given that our principal definition of allostatic load is
based on guidelines and empirical cut-points for the entire
adult population and the young ages of the women under
investigation, few women were in the high risk category of
a number of components. To allow for more variability in
allostatic load scores, we created an alternative definition
based entirely on empirical cut-points estimated from the
current sample. These alternative cut-points were: diastolic
blood pressure O 71 mmHg; systolic blood pressure O 113
mmHg; glycosolated hemoglobin > 5.3%; body mass
index O 28.3 kg/m2; triglycerides > 132 mg/dl; HDL
cholesterol < 44 mg/dl; total cholesterol O 201; albumin
< 3.9 g/dl; C-reactive protein O 0.40 mg/dl; peak
flow O 7611 ml; and creatinine clearance < 91.05 mg/dl.
Values for the alternative definition ranged from 0 to 10,
with a mean score of 3.1. High allostatic load was defined as

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TABLE 1. Characteristics of women by early age of menarche

Early menarche Not early menarche
N
Weighted N
Age (years)

214
1,782,002
23.4

Race/ethnicity
N (weighted %)
White, non-Hispanic
50 (66)
Black, non-Hispanic
85 (22)
Mexican American
70 (9)
Other
9 (3)
Marital status
Married or coupled
98 (48)
Divorced, widowed or separated
19 (7)
Never married
96 (45)
Highest level of education
11 years or less
90 (34)
12 years
65 (38)
13 years or more
59 (29)
Povertyincome ratio
00.49
24 (7)
0.50.99
59 (19)
1.01.49
27 (13)
1.501.99
21 (14)
2.0 or greater
63 (47)
Smoking history
Current smoker
50 (36)
Past smoker
23 (14)
Never smoked
141 (50)
History of depression
26 (16)

2256
23,765,096
23.8
N (weighted %)
643 (70)
733 (13)
780 (7)
100 (9)
963 (46)
174 (9)
1116 (46)
775 (24)
857 (37)
614 (38)
280 (8)
413 (14)
328 (11)
266 (13)
777 (54)
533 (32)
154 (9)
1569 (59)
233 (11)

a score in the top quartile (5 or greater). Associations with

early menarche are presented in Table 3.

Statistical Methods
The effect parameter computed was the odds ratio estimated
from a multivariable logistic regression model. Factors that
were associated with both the determinant and outcome
were evaluated as potential confounders of the allostatic
loadearly menarche association. In this analysis, race/
ethnicity (white, non-Hispanic; black, non-Hispanic;
Mexican American; other race or ethnicity), age (in years,
continuous), marital status (married; divorced, widowed or
separated; never married), years of education completed (11
years or less; 12 years; 13 or more years), poverty income
ratio for household (00.49; 0.50.99, 1.01.49; 1.51.99;
2.0 or greater); smoking history (current smoker; past
smoker; never smoked), and depression (yes/no) were
evaluated for confounding. The following were considered
in identification of confounders: biologic plausibility; prior
published evidence; and/or 10% change in estimate of the
main effect upon addition to the model. Preliminary
analyses were conducted using SAS v. 8.02 (43). SUDAAN
8.0 (PROC RLOGIST and PROC DESCRIPT) was used to

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ALLOSTATIC LOAD AND AGE AT MENARCHE

441

TABLE 2. Distribution of components of allostatic load score

Variable

High
risk
group

Cardiovascular and metabolic factors

Diastolic blood
O 90
pressure (mmHg)*
Systolic blood
O 140
pressure (mmHg)*
Glycosolated
> 5.6
hemoglobin (%)**
Body mass index
O 30
(kg/m2)*
Triglycerides
> 150
(mg/dl)y
(fasters)
> 170 (nonfasters)
HDL cholesterol
< 40
(mg/dl)*
Total cholesterol*
> 240
Inflammation markers
Albumin (g/dl)**
C-reactive protein
(mg/dl)**
Peak flow
(largest value, ml)**
Creatinine clearance
(mg/dl)**
Composite allostatic
load score

All women

Not early menarche

Mean

SD

High
risk

2456

66.4

14.4

0.7% 210

2461 107.5

12.9

2456

4.9

2466

24.3

1.0

Mean

SD

66.6

14.9

3.5% 2246

0.2% 212 109.4

14.7

SD

66.3

14.2

0.5%

0.84

0.4% 2249 107.3

12.8

0.2%

0.06

0.9

4.1%

0.16

0.6 10.2% 2243

4.9

9.4 14.4% 214

27.1

9.9 29.8% 2252

24.1

9.0 13.2%

!0.001

161.6 24.3% 2220 103.5

94.2 11.8%

0.05

27.8 13.9%

0.04

65.6

6.2%

0.01

1.4 29.0%
0.9 20.8%

0.55
0.05

2425

27.1 14.4% 211

71.1

51.7

6.7% 212 191.4

63.9 14.0% 2227 180.6

O 5922

2386 6876

3229

22.0% 211 6668

2092

26.5% 2175 6892

3190 21.6%

0.14

< 44.64

2428 144.3

135.5 11.5% 208 142.3

114.2

9.8% 2220 144.5

141.8 11.6%

0.81

2.5 18.7% 214

4.2
0.48

54.8

2412
2422

1.37

1.5 28.9% 212

1.0 21.6% 212

19.8 20.5% 2214

< 3.9
O 0.33

2470

4.1
0.38

Mean

5.0

99.6 12.7% 212 126.4

2439 181.4

Not early vs. early

menarche p-value for
difference in means

High
risk

4.5% 213

2432 105.1

54.6

Early menarche

High
risk

1.99

0.6 27.3% 2200

0.7 32.6% 2210

2.5 17.6% 2256

4.1
0.37

1.33

2.4 33.1%

!0.001

*Cutpoint determined by clinical guidelines.

**Empirically determined cut-point.
y
Combination of clinical and empirical cut-point.

incorporate the sampling weights and design effects of the

NHANES III complex sampling design (44).

RESULTS
Approximately 7% of women between the ages of 17 and 30
reported an early age of menarche. Women who experienced early menarche were similar to those who did not in
terms of age and marital status (see Table 1). However, the
prevalence of early menarche appeared higher among
women who were non-Hispanic blacks, had less than
a high school education, were current or past cigarette
smokers, or had a history of depression. Further, the
prevalence of early age at menarche was associated with
current household poverty income ratio. Women who
reported a household income two or more times the poverty
level were less likely to report early age at menarche.
Table 2 presents means and standard errors for the
individual allostatic load components as well as the percent
in the high risk category by age at menarche. The
proportion of women defined as high-risk among the

clinically determined components (blood pressure, BMI,

total and HDL cholesterol) were small, as expected, given
the young ages of the women in the analysis. The mean
values of the components were significantly different for 5 of
the 11 components. For example, the mean BMI among
women who experienced menarche at age 10 or earlier was
27.1 kg/m2 compared with 24.1 kg/m2 for those whose
menarche occurred at age 11 or older. Similarly, women
with early menarche had higher total cholesterol (191.4 vs.
180.6 mg/dl) and lower HDL cholesterol (51.7 vs. 54.8 mg/dl)
than women who did not report early menarche.
When examining the categorical variables indicating
high risk of individual components, there was a statistically
significant difference for all 11 allostatic load score
components (p-values ! 0.001). In particular, there was
a higher proportion of women with early age at menarche in
the high-risk categories compared with women who did not
report early menarche for diastolic blood pressure (4% vs.
! 1%), glycosylated hemoglobin (10% vs. 4%), BMI (30% vs.
13%), serum triglycerides (24% vs. 12%), HDL cholesterol
(21% vs. 14%), total cholesterol (14% vs. 6%), C-reactive
protein (33% vs. 21%), and peak flow (27% vs. 22%).

442

Allsworth et al.
ALLOSTATIC LOAD AND AGE AT MENARCHE

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TABLE 3. Odds of early age at menarche, odds ratios and 95% confidence intervals from crude and adjusted logistic regression models
Main allostatic load definition*
Variable

Odds ratio

95% CI

Model 1 Crude
High allostatic load score
2.42
1.543.80
Model 2 Adjusted for age
High allostatic load score
2.48
1.593.89
Age
0.97
0.921.01
Model 3 Adjusted for age, race/ethnicity, education, PIR, smoking history, and depression
High allostatic load score
2.24
1.333.77
Age
0.97
0.911.04
Race/ethnicity
Black, non-Hispanic
1.81
1.142.87
Mexican American
1.13
0.651.99
Other race/ethnicity
0.41
0.151.10
White, non-Hispanic
Ref.

Education
Less than high school
1.50
0.663.44
High school
1.10
0.552.18
More than high school
Ref.

Povertyincome ratio
0.000.49
0.64
0.291.39
0.500.99
1.86
0.844.13
1.001.49
1.01
0.482.16
1.501.99
0.93
0.352.47
2.0 or greater
Ref.

Cigarette smoking
Current smoker
1.22
0.662.25
Past smoker
1.98
1.013.88
Never smoked
Ref.

History of depression
1.60
0.872.96

Alternative allostatic load definition**

Odds ratio

95% CI

2.60

1.644.13

2.75
0.96

1.704.44
0.911.01

2.49
0.96

1.484.20
0.901.03

1.87
1.17
0.44
Ref.

1.173.00
0.682.03
0.161.17

1.48
1.06
Ref.

0.633.50
0.522.16

0.61
1.84
1.01
0.96
Ref.

0.281.33
0.824.16
0.452.23
0.362.57

1.27
1.95
Ref.
1.57

0.702.30
1.003.79

0.842.95

*Defines high risk categories from clinical guidelines and empirical cut-points from the entire adult population.
**Defines high risk categories from empirical cut-points from the current analytic sample.

Overall, approximately 22% of the women with early

ages at menarche and 32% of other women did not have
a single measure in the high risk category. Similarly, early
menarche women had a higher mean allostatic load score
(1.99 vs. 1.33, p ! 0.001). Of the women that experienced
early age at menarche, 33% also had high allostatic load
scores (3 or greater). In contrast among those that did not
experience early menarche, 17% had high allostatic load
scores.
Table 3 presents regression results from three models
estimating the association between early menarche and high
allostatic load score. The crude and age-adjusted only
models each estimated that women with high allostatic load
scores were approximately 2.4 times as likely to have
experienced early menarche as those who had lower scores.
After adjusting for age, race/ethnicity, level of education,
household poverty income ratio, smoking, and depression
history, women with high allostatic load scores had more
than two times the odds as those with low scores of
experiencing menarche at age 10 or earlier (OR Z 2.18;
95% CI, 1.293.68). Other factors associated with early
menarche were being of black, non-Hispanic race/ethnicity

or reporting a history of cigarette smoking. Finally, history of

depression, less than high school education, and current
cigarette smoking were associated with small, but not
significant, increases in the odds of early menarche.

DISCUSSION
In prior literature, the association between stress and age at
menarche has resulted in mixed findings. For instance, in
a study of adolescents in Bosnia (21), traumatic events
delayed menarche, while a study by Campbell and
colleagues (22) of California examined behavior symptoms
of elevated stress and found no association with age at
menarche. In contrast, Kim and Smith (19) found that
earlier age of menarche was associated with stress in family
life between the ages of 7 and 11 as well as with indicators of
poor relationships with mothers. Similarly, Hulanicka and
colleagues (20) reported that the mean age of menarche was
0.4 years earlier for girls living in families that had
experienced prolonged stress than for those with families
free of major traumatic events (12.9 vs. 13.3 years).

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In our study, the first to examine the relationship between womens age at menarche with allostatic load, women
with high allostatic load scores were twice as likely to
experience early menarche as those with lower scores. These
analyses were conducted using data from a national probability sample of US women collected by the NHANES III
survey. Following adjustment with individual sampling
weights, our findings are representative of the population
of US women between the ages of 17 and 30 at the time of
the survey.
There are a number of limitations that should be
considered in the interpretation of these findings. First, the
study design is cross-sectional and therefore does not imply
causality. This association could have also been observed if
an unobserved independent biologic process was associated
with both age at menarche and composite allostatic load
score. A second alternative explanation is that early age at
menarche causes greater increases in allostatic load scores as
women age than would be anticipated by the normal aging
process (38). To explore this possibility, we conducted
additional analyses that were limited to 1) women who had
experienced menarche in the past 10 years or 2) women aged
25 years or younger; such analyses did not support this
alternative explanation (data not presented). In fact, among
these women, the association of high allostatic load score
and early menarche was slightly stronger. However, due to
the cross-sectional design of this sample, concerns about
temporal sequence cannot be ruled out.
A third potential limitation, differential recall of age at
menarche, could have been an important factor in the
interpretation of our results. A previous study of adolescents,
however, found substantial correlation with self-reported
age at menarche with medical records (45). Furthermore,
a subsample analysis of the current study including only
women under the age of 25 years, found similar results to
those presented here (data not presented). Finally, due to
the data available as part of NHANES III, the current
definition of allostatic load was based on that of Crimmins
and colleagues (38) which included clinical measurements
from multiple physiologic systems, and as such does not
include direct measurement of stress biomarkers.
The concept of allostatic load may prove an important
one for fully understanding influences on womens reproductive health. Early age at menarche in addition to its
association with reproductive aging is also a risk factor for
cardiovascular and other diseases in later life. Although
allostatic load measures have been predominatly applied to
aging populations (30, 32, 33, 36, 38), this study demonstrates the utility of measuring and analyzing the effect of
allostatic load in young populations as well. Future studies
involving prospective measurement of allostatic load
biomarkers will be essential for disentangling the association
between allostatic load and early age at menarche.

Allsworth et al.
ALLOSTATIC LOAD AND AGE AT MENARCHE

443

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